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Contribution of Ipsilateral Primary Motor Cortex Activity to the Execution of Voluntary Movements in Humans: a Review of Recent Studies

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Contribution of Ipsilateral Primary Motor Cortex Activity to the Execution of Voluntary Movements in Humans: a Review of Recent Studies J Phys Fitness Sports Med, 3(3): 297-306 (2014) DOI: 10.7600/jpfsm.3.297 JPFSM: Review Article Contribution of ipsilateral primary motor cortex activity to the execution of voluntary movements in humans: A review of recent studies Kazumasa Uehara1,2 and Kozo Funase1* 1 Human Motor Control Laboratory, Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8521, Japan 2 Japan Society for the Promotion of Science, 8 Ichiban-cho, Chiyoda-ku, Tokyo 102-8472, Japan Received: May 13, 2014 / Accepted: May 29, 2014 Abstract In primates, unilateral voluntary movements are preferentially controlled by the primary motor cortex (M1) contralateral to the side performing the movement. However, it has been reported that the M1 ipsilateral to the side performing the movement (ipsi-M1) is also activated during unilateral voluntary movements. Recently, studies involving transcranial magnetic stimulation (TMS) or functional magnetic resonance imaging (fMRI) techniques have gradually elucidated the neural mechanisms responsible for modulating ipsi-M1 activity. In particular, the modulation of ipsi-M1 activity is likely to occur in a task-dependent manner, and is also closely associated with advancing age. In addition, ipsi-M1 excitability is suppressed during the acquisition phase of motor learning. Previous studies have suggested that the modu- lation of ipsi-M1 activity occurs via changes in the activation of the corpus callosum pathways linking the bilateral M1. In this article, we will broadly review the features of ipsi-M1 activity, observed during the execution of unilateral movements, as well as the detailed neural mecha- nisms underlying the modulation of ipsi-M1 activity. Understanding the role played by ipsi-M1 activity during voluntary movements would improve our knowledge of human motor control systems. Keywords : ipsilateral primary motor cortex, voluntary movement, task-dependency, corpus cal- losum, human motor control, motor learning pass perpendicular to the plane of the coil, which induces Introduction eddy currents within the brain. When suprathreshold TMS During unilateral voluntary movements involving the is delivered over the M1 representation of hand muscles, upper limbs, the muscles in the upper limbs are predomi- the magnetic pulse evokes a muscle response in the con- nantly under the control of crossed corticospinal tracts tralateral hand muscle, which can be recorded using elec- originating from the primary motor cortex contralateral tromyography12). Such muscle responses are called motor (contra-M1) to the side performing the movement, be- evoked potentials (MEP). The TMS technique is widely cause approximately 80% of corticospinal fibers cross used to assess neurophysiological changes in M1 excit- over to the contralateral side at the pyramidal decussa- ability. On the other hand, fMRI is a non-invasive high tion1). However, there is a growing body of evidence to spatial resolution mapping method in which MRI signals suggest that the ipsilateral M1 (ipsi-M1) is also involved are used to detect blood flow and oxygen metabolism as in controlling upper limb movements (Fig. 1)2-11). a means of measuring the neural activity of the whole Due to recent developments in neuroimaging, e.g., brain13,14). Ogawa et al.15) were the first to demonstrate the functional magnetic resonance imaging (fMRI), and neu- blood oxygen level dependent (BOLD) signals that are rophysiological techniques, e.g., transcranial magnetic the basis of the fMRI technique. The blood oxygen levels stimulation (TMS), findings regarding the features of ipsi- within particular areas of the brain are remarkably sensi- M1 activity, induced during unilateral movements, and tive to the changes in neural activity induced by motor, the mechanisms by which ipsi-M1 activity is modulated motor imagery, or cognitive tasks. As with the TMS tech- have been reported since the late 1990s. In brief, TMS nique, fMRI has been widely used across a range of re- is a non-invasive brain stimulation technique in which search fields to assess brain and spinal activity in humans. neurons are temporarily activated using a magnetic coil. A representative TMS study by Stedman et al.2) found A magnetic field is produced within the lines of flux that that MEPs, induced in a relaxed finger muscle in response to single-pulse TMS of the contra-M1, were increased *Correspondence: [email protected] when the opposite homologous muscle was voluntarily 298 JPFSM: Uehara K and Funase K Ipsilateral hemisphere Contralateral hemisphere (resting M1) (active M1) Corpus callosum pathway Spinal Fig. 1 A schematic illustration of the descending tracts motoneuron (black arrows) originating from the M1 and the corpus callosum pathways (blue arrow) connect- ing both hemispheres. In general, unilateral vol- untary movements are preferentially controlled by the M1 contralateral to the movement side. However, the M1 ipsilateral to the movement side is also involved in unilateral movements. The corpus callosum pathways could be one of the pathways involved in the modulation of ipsi- M1 activity. Movement side activated. It is suggested that such increases in the MEPs Given the accumulating evidence regarding the effects of relaxed finger muscles probably result from both corti- of ipsi-M1 activity during voluntary movements, we con- cal and spinal activity. In a study using fMRI, Kobayashi sider that activation of the ipsi-M1 during unilateral vol- et al.16) reported that during a repetitive unilateral rhyth- untary movements is worthy of attention from researchers mic movement, activation of both the contra- and ipsi- investigating human motor control systems. The primary M1 was detected in half of the participants. According to goal of this article is to review the contribution of ipsi-M1 the studies described above, the execution of unilateral activity and the neural mechanisms underlying the modu- voluntary movements involving the upper limbs is ac- lation of ipsi-M1 excitability during various voluntary companied by an increase in ipsi-M1 excitability. Studies movement tasks involving the use of the upper limbs. In examining the mechanisms responsible for such changes addition, we will review the relationship between aging have reported that modulation of the corpus callosum and ipsi-M1 activity and the role played by ipsi-M1 activ- pathways linking both hemispheres7,10,16-19) or ipsilateral ity in motor learning. Furthermore, we will discuss the projections to the ipsilateral spinal cord20) are involved functional significance of ipsi-M1 activity during unilat- in MEP changes in the opposite limb during the perfor- eral movement. mance of unilateral movements. Very recently, it has been reported that uncrossed descending pathways originating Task-dependent modulation of ipsi-M1 activity from the ipsi-M1 to the ipsilateral spinal cord play an im- portant role in controlling skilled upper limb movement In recent human TMS studies examining the relation- as well as selective muscle activity in the proximal upper ship between simple muscle contractions and ipsi-M1 ex- limb21-23). citability, it was reported that unilateral isometric muscle In addition, clinical evidence has been obtained regard- contractions of the wrist or finger muscles significantly ing the contribution of the ipsi-M1 to post-stroke recov- increase the excitability of the ipsi-M1 for the opposite ery. Specifically, it has been suggested that upregulation homologous muscle and that the degree of ipsi-M1 excit- of the activity of the contralesional M1 (i.e., ipsilateral to ability increased with muscle contraction strength8,17,18,26). the paretic side) might be important for improving paretic With regard to muscle contraction type, a previous study arm function after stroke24,25). These findings indicate that assessed the changes in the MEP induced in the relaxed the M1 ipsilateral to the paretic side discharges neural im- opposite flexor carpi radialis (FCR) during shortening or pulses to the paretic limb via either uncrossed descending lengthening muscle contractions of the forearm muscles. or corpus callosum pathways on behalf of the ipsilesional As a result, it was found that of the MEP evoked in the M1. relaxed FCR during the lengthening muscle contractions JPFSM: Contribution of ipsilateral motor cortex to human motor control 299 exhibited significantly smaller amplitudes than those have also been studied using TMS. As a result, an in- evoked during the shortening muscle contractions27), indi- crease in ipsi-M1 excitability was detected during the ex- cating that muscle contraction type affects ipsi-M1 excit- ecution of a unilateral imagined voluntary movement of ability. Thus, even during the execution of simple muscle the index finger28). Furthermore, a relationship was dem- contraction tasks, ipsi-M1 excitability is affected by the onstrated to exist between the inhibitory corpus callosum strength and type of the contractions. pathways connecting the bilateral M1, i.e., interhemi- The relationship between the performance of skilled spheric inhibition (IHI), and motor imagery. Specifically, motor tasks involving the finger muscles and ipsi-M1 the IHI from the contra- to the ipsi-M1 was significantly activation has been established. Morishita et al. assessed increased during unilateral imagined voluntary movement ipsi-M1 excitability using single-pulse TMS while right- compared with that observed during the resting state (i.e.,
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